Role of olfaction in the conditioned sucrose preference of sweet-ageusic T1R3 knockout mice

Abstract

Prior work has shown that sweet taste-deficient T1R3 knockout (KO) mice developed significant sucrose preferences when given long-term sugar versus water tests. The current study investigated the role of olfaction in this experience-conditioned sucrose preference. T1R3 KO and C57BL/6 wild-type (WT) mice were given 24-h sugar versus water tests with ascending concentrations of sucrose (0.5-32%), after which the mice received olfactory bulbectomy (OBx) or sham surgery. When retested with sucrose, the Sham-KO mice preferred all sugar solutions to water, although their intake and preference were less than those of the Sham-WT mice. The OBx-KO mice, in contrast, showed no or weak preferences for dilute sucrose solutions (0.5-8%) although they strongly preferred concentrated sugar solutions (16-32%). OBx-WT mice displayed only a partial reduction in their sucrose preference. Although the OBx mice of both genotypes underconsumed dilute sucrose solutions relative to Sham mice, they overconsumed concentrated sucrose. These results indicate that olfaction plays a critical role in the conditioned preference of T1R3 KO mice for dilute sugar solutions. Further, the fact that OBx-KO mice preferred concentrated sucrose solutions in the absence of normal sweet taste and olfactory sensations underscores the potency of postoral nutritive signals in promoting ingestion.

Figure 1

Sucrose solution intake (±standard error of the mean) (top panel) and percent sucrose preference (bottom panel) of Sham-KO and Sham-WT mice during sucrose versus water 2-bottle Tests 1 and 2. Water intakes are not shown. Ten days intervened between the 2 tests during which sham surgery was performed. Significant (P < 0.05) genotype differences at individual concentrations are indicated by an asterisk. The lowest concentration at which sucrose was significantly preferred to water is indicated by a plus sign.

Figure 2

Sucrose solution intake (±standard error of the mean) (top panel) and percent sucrose preference (bottom panel) of OBx-KO and OBx-WT mice during sucrose versus water 2-bottle Tests 1 and 2. Water intakes are not shown. Ten days intervened between the 2 tests during which OBx surgery was performed. Significant (P < 0.05) genotype differences at individual concentrations are indicated by an asterisk. The lowest concentration at which sucrose was significantly preferred to water is indicated by a plus sign.

Figure 3

Sucrose solution intake (±standard error of the mean) (top panels) and percent sucrose preference (bottom panels) of Sham-WT and OBx-WT mice (left panels) and Sham-KO and OBx-KO mice (right panels) during sucrose versus water 2-bottle Test 2. Water intakes are not shown. Significant (P < 0.05) within-genotype differences at individual concentrations are indicated by an asterisk. The lowest concentration at which sucrose was significantly preferred to water is indicated by a plus sign.

Figure 4

Sucrose solution intake (±standard error of the mean) (top panel) and percent sucrose preference (bottom panel) of OBx-KO, OBx-WT, Sham-KO, and Sham-WT mice during 24-h 0.5% sucrose versus water 2-bottle Test 3 using food-grade and reagent-grade sugar. Water intakes are not shown.

Figure 5

Odor avoidance Test 5. CS+/LiCl and CS−/NaCl solution intakes (+standard error of the mean) during 1-bottle training and CS+/NaCl and CS−/NaCl intake during 2-bottle test of OBx-KO, OBx-WT, Sham-KO, and Sham-WT mice. CS+ refers to the odor added to LiCl during training but added to NaCl during testing. CS- refers to the odor added to NaCl during training and testing. Significant (P < 0.05) differences between CS+ versus CS− odorized solutions are indicated by an asterisk. Numbers atop bars in 2-bottle tests are the percent CS+/NaCl.

Figure 6

Schematic representation of the extent of the smallest (cross-hatched) and largest (hatched) OBx lesions in the OBx-KO and OBx-WT groups. Anatomical landmarks of the intact brain are indicated in the top diagram: AON; cc, corpus callosum; FC, frontal cortex; OB, olfactory bulb; S, striatum.